Abstract
The regular firing pattern exhibited by medial entorhinal (mEC) grid cells of locomoting rodents is hypothesized to provide spatial metric information relevant for navigation. The development of virtual reality (VR) for head-fixed mice confers a number of experimental advantages and has become increasingly popular as a method for investigating spatially-selective cells. Recent experiments using 1D VR linear tracks have shown that some mEC cells have multiple fields in virtual space, analogous to grid cells on real linear tracks. We recorded from the mEC as mice traversed virtual tracks featuring regularly spaced repetitive cues and identified a population of cells with multiple firing fields, resembling the regular firing of grid cells. However, further analyses indicated that many of these were not, in fact, grid cells because: (1) when recorded in the open field they did not display discrete firing fields with six-fold symmetry; and (2) in different VR environments their firing fields were found to match the spatial frequency of repetitive environmental cues. In contrast, cells identified as grid cells based on their open field firing patterns did not exhibit cue locking. In light of these results we highlight the importance of controlling the periodicity of the visual cues in VR and the necessity of identifying grid cells from real open field environments in order to correctly characterize spatially modulated neurons in VR experiments.
Highlights
Since their discovery, the striking regularity of grid cell firing patterns has been proposed to play a role in encoding traveled distances and are widely held to be a core component of a circuit necessary for the integration of self-motion cues—‘‘path integration’’ (Hafting et al, 2005; McNaughton et al, 2006; Burgess, 2008; Burak and Fiete, 2009; Winter et al, 2015)
Only 7/56 of the periodic cells were not cue-locked in at least one of the three environments, with 16/56 being cue-locked in one environment, 27/56 in two environments and 6/56 in all three environments (Figure 3C). These results suggest that the regular firing pattern exhibited by these periodic cells was strongly modulated by the repeating visual cues rather than reflecting an internallygenerated path integration signal like the one hypothesized for grid cells
The core finding presented here is the report of a distinct population of neurons in rodent mEC characterized by robust modulation of their firing rate by visual cues presented in linear virtual reality (VR) environments—‘‘cue-locked’’ cells
Summary
The striking regularity of grid cell firing patterns has been proposed to play a role in encoding traveled distances and are widely held to be a core component of a circuit necessary for the integration of self-motion cues—‘‘path integration’’ (Hafting et al, 2005; McNaughton et al, 2006; Burgess, 2008; Burak and Fiete, 2009; Winter et al, 2015). Manipulations made to familiar spatial cues result in commensurate changes to grid-patterns (Hafting et al, 2005; Barry et al, 2007; Stensola et al, 2012), in geometrically polarized environments firing is distorted (Krupic et al, 2015, 2018; Stensola et al, 2015), and in darkness their spatially periodic activity can break down completely (Chen et al, 2016; Pérez-Escobar et al, 2016) It appears that while grid cell activity is shaped by self-motion information (Winter et al, 2015), sensory access to landmarks is necessary to maintain stable spatial firing (Hardcastle et al, 2015; Muessig et al, 2015; Campbell et al, 2018). When rats first explored a pair of visually identical enclosures connected by a corridor, grid cell firing in the enclosures was highly similar, suggesting a dominance of
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